Inbreeding and Endangered Species Management: Is New Zealand Out of Step with the Rest of the World? IAN G. JAMIESON,∗‡ GRAHAM P. WALLIS,∗ AND JAMES V. BRISKIE† ∗Department of Zoology, University of Otago, P.O. Pox 56, Dunedin, New Zealand †School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand Abstract: There is growing evidence that inbreeding can negatively affect small, isolated populations. This contrasts with the perception in New Zealand, where it has been claimed that native birds are less affected by inbreeding depression than threatened species from continental regions. It has been argued that New Zealand’s terrestrial birds have had a long history of small population size with frequent inbreeding and that this has “purged” deleterious alleles. The rapid recovery of many tiny and inbred populations after introduced predators have been controlled, and without input from more genetically diverse populations, has further supported the view that inbreeding is not a problem. This has led to a general neglect of inbreeding as a factor in recovery programs for highly endangered species such as the Black Robin ( Petroica traversi) and Kakapo ( Strigops habroptilis). We examined the reasons for this situation and review the New Zealand evidence for genetic purging. Complete purging of the genetic load and elimination of inbreeding depression are unlikely to occur in natural populations, although partial purging may be more likely where small populations have become inbred over an extended period of time, such as on small isolated islands. Recent molecular data are consistent with the view that island endemics, including New Zealand’s threatened birds, have low genetic variation and hence have possibly gone through longer periods of inbreeding than threatened species from continental regions. Nevertheless, results from recent field studies in New Zealand indicate that, despite the opportunity for purging, inbreeding depression is evident in many threatened species. Although inbreeding depression has not prevented some populations from recovering from severe bottlenecks, the long-term consequences of inbreeding and small population size—the loss of genetic variation—are potentially much more insidious. The degrees to which genetic factors reduce population viability generally remain unquantified in New Zealand. Although minimizing ecological risks (e.g., preventing reinvasion of islands by mammalian predators) will continue to receive high priority in New Zealand because of their much larger impacts, we advocate that genetic considerations be better integrated into recovery plans. Key Words: Black Robin, genetic purging, Kakapo, Takahe Endogamia y Gesti´on de Especies en Peligro: ¿Est´a Nueva Zelanda Desfasada del Resto del Mundo? Resumen: Cada vez hay mas´ evidencias de que la endogamia puede afectar negativamente a poblaciones pequenas˜ aisladas. Esto contrasta con la percepcion´ en Nueva Zelanda, donde se ha afirmado que la en- dogamia tiene menos efecto sobre las aves nativas que sobre las especies amenazadas de regiones continen- tales. Se ha argumentado que las aves terrestres de Nueva Zelanda tienen una larga historia de poblaciones pequenas˜ con endogamia frecuente y que esto ha “purgado” alelos delet´ereos. La rapida´ recuperacion´ de muchas poblaciones pequenas˜ y endogamicas´ despu´es de que se ha controlado a depredadores introducidos, y sin entradas desde poblaciones mas´ diversas gen´eticamente, ha reforzado la idea de que la endogamia no es un problema. Esto ha llevado a la desatencion´ general de la endogamia como un factor en los programas de re- cuperacion´ de especies en peligro cr´ıtico como Petroica traversa y Strigops habroptilis. Examinamos las razones de esta situacion´ y revisamos la evidencia de purga gen´etica en Nueva Zelanda. Es poco probable que haya una purga completa de la carga gen´etica y eliminacion´ de la endogamia en poblaciones naturales, aunque ‡email [email protected] Paper submitted April 1, 2004; revised manuscript accepted March 29, 2005. 38 Conservation Biology Volume 20, No. 1, 38–47 C 2006 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2006.00282.x Jamieson et al. Inbreeding in New Zealand Birds 39 es mas´ probable que haya purgas parciales donde las poblaciones han sido endogamicas´ durante extensos per´ıodos de tiempo, tal como en pequenas˜ islas aisladas. Datos moleculares recientes son consistentes con la idea de que especies end´emicas a islas, incluyendo las especies de aves amenazadas de Nueva Zelanda, tienen variacion´ gen´etica baja y por lo tanto es posible que hayan tenido per´ıodos de endogamia mas´ prolongados que los de especies de regiones continentales. Sin embargo, los resultados de estudios de campo recientes en Nueva Zelanda indican que, a pesar de la oportunidad de purga, la endogamia es evidente en muchas especies amenazadas. Aunque la endogamia no ha impedido que algunas especies se recuperen de cuellos de botella severos, las consecuencias a largo plazo de la endogamia y del tamano˜ poblacional pequeno˜ – la p´erdida de variacion´ gen´etica – son potencialmente mas´ insidiosas. El grado en que los factores gen´eticos reducen la viabilidad poblacional en general no esta´ cuantificado en Nueva Zelanda. Aunque la minimizacion´ de los riesgos ecologicos´ (e.g., prevenir la reinvasion´ de mam´ıferos depredadores en las islas) seguira´ teniendo alta prioridad en Nueva Zelanda debido a su mayor impacto, recomendamos que los temas gen´eticos sean considerados en los planes de recuperacion.´ Palabras Clave: Petroica traversi, Porphyrio mantelli, purga gen´etica, Strigops habroptili Introduction nowhere more evident than in New Zealand. Hunting and forest burning by early Polynesians eliminated more than Habitat loss and invasive species are considered the pri- 35% of endemic land birds, and further land clearance mary drivers of population extinction. There is grow- and widespread introduction of exotic mammals (partic- ing evidence, however, that inbreeding depression can ularly rats, mustelids, and cats) by Europeans threatened further affect wild populations once they become small much of the surviving fauna (Duncan & Blackburn 2004). (Crnokrak & Roff 1999; Hedrick & Kalinowski 2000; Because the endemic fauna evolved in the absence of ter- Keller & Waller 2002). Empirical studies have confirmed restrial mammals, the overriding focus for recovery of en- direct links between inbreeding and/or loss of genetic dangered populations is limiting predation by introduced variation and population viability (e.g., Westemeier et al. mammals (Clout 2001). Although many species of en- 1998; Madsen et al. 1999). In a recent review of the liter- demic birds, frogs, and invertebrates are characterized by ature, Keller and Waller (2002) concluded that inbreed- low population numbers, range contraction, and severe ing and inbreeding depression occur commonly in nature population fragmentation, reduced genetic variation and and can be severe enough to affect the viability of small inbreeding are often seen as inconsequential when behav- and isolated populations, especially those of endangered iorally na¨ıve endemics are faced with repeated outbreaks species. of carnivorous rats, stoats, or feral cats. Managers tend The New Zealand avifauna has one of the highest pro- to focus efforts on restoration programs that establish portions of endangered species for its landmass (Bell small populations on offshore islands free of introduced 1991), yet only 1 of the 13 bird studies listed by Keller predators and are less concerned about long-term conse- and Waller (2002) as an example of inbreeding depres- quences of inbreeding (Armstrong & McLean 1995). sion comes from New Zealand. New Zealand’s endan- Although predation by exotic mammals has led to the gered bird populations have a long history of intensive extinction and fragmentation of many native species, the study (Bell 1991) yet are conspicuous by their absence in argument that genetic factors are unimportant relative to the inbreeding literature. If inbreeding depression is im- introduced predators is misplaced. Inbreeding effects op- portant in reducing persistence probability of small pop- erate on a longer time scale (generations) than ecological ulations, we would expect the negative consequences of effects (years) (Soul´e & Mills 1998). Even if conservation inbreeding to be evident in New Zealand’s well-studied measures succeed at controlling direct threats such as in- and highly endangered bird fauna. In this essay we ex- troduced predators, inbreeding and loss of genetic varia- plore why New Zealand conservation biologists appear tion may ultimately lead to extinction. Therefore genetic less likely to focus on genetic factors when implement- factors could be influencing demographic processes af- ing recovery plans for the country’s threatened avifauna. fecting population persistence in New Zealand, but they could be less obvious than the effects of habitat destruc- tion and depredation by exotic mammals. Causal Factors of Population Decline in New Zealand The Role of Inbreeding in New Zealand Species Few would disagree that on an ecological time scale the By focusing more on the ecological agents of declining greatest risks of extinction to small populations come pri- populations than on genetic consequences once pop- marily from habitat loss and introduced predators. This is ulations become small (Caughley 1994), conservation Conservation Biology Volume